Age and sex-related changes in the structure and strength of the human femoral shaft

Martin, R. Bruce; Atkinson, Peter J.

Affiliations

¹West Virginia University Medical Center, Morgantown, VA 26506, U.S.A.

²Department of Oral Biology, School of Dentistry, the University of Leeds, Leeds, L52 9NZ England

Abstract

In order to quantify age-related changes in the structural integrity of the human femur, data from four sites on each of 37 left femoral shafts was analyzed. Measurements of bone specific gravity were converted to estimates of material strength in bending using empirical relations reported in the literature. Structural strength was determined by measuring cross-sectional moments of inertia. These data were then used to calculate the bending strength of the femoral shaft as functions of position, age, and sex.

The results indicate that the material strength of femoral bone decreases with age equally in males and females. In males this decrease is compensated by increases in section modulus so that the overall strength of the shaft remains constant. In females, the section modulus decreases with age, exacerbating the effects of material weakness and leading to greatly reduced femoral strength in old age. These results are supported by related experimental evidence from the literature. Additional useful engineering data on the structural properties of the femoral shaft are also reported.

Links

DOI: 10.1016/0021-9290(77)90045-8

PubMed: 858728

WoS: A1977DG31500002

History

Received: 1976-08-24

Cited Works (11)

Year	Entry
1968	Currey JD. The adaptation of bones to stress. J Theo Biol. July 1968;20(1):91-106.
1966	Sedlin‌ ED, Hirsch C. Factors affecting the determination of the physical properties of femoral cortical bone. Acta Orthop Scand. 1966;37(1):29-48.
1967	Atkinson PJ, Weatherell JA. Variation in the density of the femoral diaphysis with age. J Bone Joint Surg. November 1967;49B(4):781-788.
1880	Messerer O. Über Elasticität und Festigkeit der menschlichen Knochen. Stuttgart, Germany: Cotta; 1880.
1972	Rybicki EF, Simonen FA, Weis EB Jr. On the mathematical analysis of stress in the human femur. J Biomech. March 1972;5(2):203-215.
1970	Abendschein W, Hyatt GW. Ultrasonics and selected physical properties of bone. Clin Orthop Relat Res. March–April 1970;69:294-301.
1968	Mather BS. Variation with age and sex in strength of the femur. Med Biol Eng. 1968;6(2):129-132.
1976	Burstein AH, Reilly DT, Martens M. Aging of bone tissue: mechanical properties. J Bone Joint Surg. 1976;58A(1):82-86.
1964	Smith RW Jr, Walker RR. Femoral expansion in aging women: implications for osteoporosis and fractures. Science. July 10, 1964;145(3628):156-157.
1960	Jowsey J. Age changes in human bone. Clin Orthop. 1960;17:210-218.
1969	Evans FG, Vincentelli R. Relation of collagen fiber orientation to some mechanical properties of human cortical bone. J Biomech. 1969;2(1):63-73.

Cited By (54)

Year	Entry
1981	Torzilli PA, Burstein AH, Takebe K, Zika JC, Heiple KG. The material and structural properties of maturing bone. In: Cowin SC, ed. Mechanical Properties of Bone. The Joint ASME-ASCE Applied Mechnics, Fluids Engineering and Bioengineering Conference; June 22-24, 1981; Boulder, CO. New York, NY: American Society of Mechical Engineers; 1981:145-161.
1988	Lane JM, Cornell CN, Healey JH. Orthopaedic consequences of osteoporosis. In: Riggs BL, Melton LJ III, eds. Osteoporosis: Etiology, Diagnosis, and Management. New York, NY: Raven Press; 1988:433-455.
1998	Martin RB, Burr DB, Sharkey NA. Skeletal Tissue Mechanics. New York, NY: Springer-Verlag; 1998.
2006	Augat P, Schorlemmer S. The role of cortical bone and its microstructure in bone strength. Age Ageing. September 2006;35(suppl 2):ii27-ii31.
1983	Ruff CB, Hayes WC. Cross‐sectional geometry of Pecos Pueblo femora and tibiae: a biomechanical investigation, I: method and general patterns of variation. Am J Phys Anthropol. 1983;60(3):359-381.
1983	Ruff CB, Hayes WC. Cross‐sectional geometry of Pecos Pueblo femora and tibiae: a biomechanical investigation, II: sex, age, and side differences. Am J Phys Anthropol. 1983;60(3):383-400.
2001	Donahue SW, Jacobs CR, Donahue HJ. Flow-induced calcium oscillations in rat osteoblasts are age, loading frequency, and shear stress dependent. Am J Physiol Cell Physiol. November 2001;281(5):C1635-C1641.
2004	Yeni YN, Dong XN, Fyhrie DP, Les CM. The dependence between the strength and stiffness of cancellous and cortical bone tissue for tension and compression: extension of a unifying principle. Bio-med Mater Eng. 2004;14(3):303-310.
1989	Carando S, Portigliatti Barbos M, Ascenzi A, Boyde A. Orientation of collagen in human tibial and fibular shaft and possible correlation with mechanical properties. Bone. 1989;10(2):139-142.
1990	Mosekilde L, Mosekilde L. Sex differences in age-related changes in vertebral body size, density and biomechanical competence in normal individuals. Bone. 1990;11(2):67-73.
1990	Jee WSS, Mori S, Li XJ, Chan S. Prostaglandin E₂ enhances cortical bone mass and activates intracortical bone remodeling in intact and ovariectomized female rats. Bone. 1990;11(4):253-266.
1993	van der Meulen MCH, Beaupré GS, Carter DR. Mechanobiologic influences in long bone cross-sectional growth. Bone. July–August 1993;14(4):635-642.
1996	Carter DR, Van der Meulen MCH, Beaupré GS. Mechanical factors in bone growth and development. Bone. January 1996;18(1)(suppl 1):S5-S10.
2000	Fyhrie DP, Vashishth D. Bone stiffness predicts strength similarly for human vertebral cancellous bone in compression and for cortical bone in tension. Bone. February 2000;26(2):169-173.
2022	Bolger MW, Romanowicz GE, Bigelow EMR, Ward FS, Ciarelli A, Jepsen KJ, Kohn DH. Divergent mechanical properties of older human male femora reveal unique combinations of morphological and compositional traits contributing to low strength. Bone. October 2022;163:116481.
1992	Beck TJ, Ruff CB, Scott WW Jr, Plato CC, Tobin JD, Quan CA. Sex differences in geometry of the femoral neck with aging: a structural analysis of bone mineral data. Calcif Tiss Int. January 1992;51(1):24-29.
1993	Beck TJ, Ruff CB, Bissessur K. Age-related changes in female femoral neck geometry: implications for bone strength. Calcif Tiss Int. 1993;53(suppl 1):S41-S46.
1994	Bouxsein ML, Myburgh KH, van der Meulen MCH, Lindenberger E, Marcus R. Age-related differences in cross-sectional geometry of the forearm bones in healthy women. Calcif Tiss Int. February 1994;54(2):113-118.
2010	Willinghamm MD, Brodt MD, Lee KL, Stephens AL, Ye J, Silva MJ. Age-related changes in bone structure and strength in female and male BALB/c mice. Calcif Tiss Int. June 2010;86(6):470-483.
1980	Martin RB, Pickett JC, Zinaich S. Studies of skeletal remodeling in aging men. Clin Orthop Relat Res. June 1980;149:268-282.
1982	Leichter I, Margulies JY, Weinreb A, Mizrahi J, Robin GC, Conforty B, Makin M, Bloch B. The relationship between bone density, mineral content, and mechanical strength in the femoral neck. Clin Orthop Relat Res. March 1982;163:272-281.
2016	Osterhoff G, Morgan EF, Shefelbine SJ, Karim L, McNamara LM, Augat P. Bone mechanical properties and changes with osteoporosis. Injury. June 2016;47(suppl 2):S11-S20.
1980	Nagurka ML, Hayes WC. An interactive graphics package for calculating cross-sectional properties of complex shapes. J Biomech. 1980;13(1):59-64.
1985	Keller TS, Lovin JD, Spengler DM, Carter DR. Fatigue of immature baboon cortical bone. J Biomech. 1985;18(4):297-304.
1989	Keller TS, Spengler DM. Regulation of bone stress and strain in the immature and mature rat femur. J Biomech. 1989;22(11-12):1115-1127.
1991	Martin RB. Determinants of the mechanical properties of bones. J Biomech. 1991;24(suppl 1):79-88.
1997	Les CM, Stover SM, Keyak JH, Taylor KT, Willits NH. The distribution of material properties in the equine third metacarpal bone serves to enhance sagittal bending. J Biomech. April 1997;30(4):355-361.
2000	Beck TJ, Looker AC, Ruff CB, Sievanen H, Wahner HW. Structural trends in the aging femoral neck and proximal shaft: analysis of the third national health and nutrition examination survey dual‐energy x‐ray absorptiometry data. J Bone Miner Res. December 2000;15(12):2297-2304.
2001	Beck TJ, Oreskovic TL, Stone KL, Ruff CB, Ensrud K, Nevitt MC, Genant HK, Cummings SR. Structural adaptation to changing skeletal load in the progression toward hip fragility: the study of osteoporotic fractures. J Bone Miner Res. June 2001;16(6):1108-1119.
2001	Duan Y, Turner CH, Kim B-T, Seeman E. Sexual dimorphism in vertebral fragility is more the result of gender differences in age-related bone gain than bone loss. J Bone Miner Res. December 2001;16(12):2267-2275.
2003	Duan Y, Beck TJ, Wang X-F, Seeman E. Structural and biomechanical basis of sexual dimorphism in femoral neck fragility has its origins in growth and aging. J Bone Miner Res. October 2003;18(10):1766-1774.
1993	Bonadio J, Jepsen KJ, Mansoura MK, Jaenisch R, Kuhn JL, Goldstein SA. A murine skeletal adaptation that significantly increases cortical bone mechanical properties: implications for human skeletal fragility. J Clin Invest. October 1993;92(4):1697-1705.
1988	Ruff CB, Hayes WC. Sex differences in age‐related remodeling of the femur and tibia. J Orthop Res. November 1988;6(6):886-896.
1982	Ruff CB, Hayes WC. Subperiosteal expansion and cortical remodeling of the human femur and tibia with aging. Science. September 3, 1982;217(4563):945-948.
2024	Szabo E. Insights Into the Mechanical Behavior of Maturing Cortical Bone: A Porcine Model [PhD thesis]. Cleveland, OH: Case Western Reserve University; May 2024.
2022	Senwar B. Bone Material Quality, Structure, and Functional Relationships Contribute to Bone Strength and Toughness [Master's thesis]. University of Colorado; 2022.
2008	Tommasini SM. Phenotypic Integration Contributes to Skeletal Functionality and Fragility [PhD thesis]. New York, NY: The City University of New York; 2008.
2007	Voide R. Functional Phenotyping of Bone: A Hierarchical Assessment of Bone Failure Characteristics [PhD thesis]. Swiss Federal Institute of Technology Zürich; 2007.
1994	Courtney AC. Mechanical Properties of the Proximal Femur: Changes With Age [PhD thesis]. Cambridge, MA: Harvard University; May 1994.
2002	Kontulainen S. Training, Detraining and Bone: Effect of Exercise on Bone Mass and Structure With Special Reference to Maintenance of the Exercise-Induced Bone Gain [PhD thesis]. University of Jyväskylä; 2002.
1998	Robling AG. Histomorphometric Assessment of Mechanical Loading History from Human Skeletal Remains: The Relation Between Micromorphology and Macromorphology At the Femoral Midshaft [PhD thesis]. University of Missouri; December 1998.
1993	van der Meulen MCH. The Influence of Mechanics on Long Bone Development and Adaptation [PhD thesis]. Stanford University; June 1993.
1998	Mandell JA. Load Transfer in Cementless Intramedullary Prostheses [PhD thesis]. Stanford University; March 1998.
2006	Carpenter RD. Mechanobiology of Bone Cross-Sectional Development, Adaptation, and Strength [PhD thesis]. Stanford University; June 2006.
2003	Fox JC. Biomechanics of the Proximal Femur: Role of Bone Distribution and Architecture [PhD thesis]. Berkeley, CA: Berkeley, University of California; 2003.
1987	Stover SM. Dorsal Metacarpal Disease in Thoroughbred Horses: Relationship to the Development of the Third Metacarpal Bone [PhD thesis]. Davis, University of California; 1987.
1994	Jepsen KJ. Characterization of the Hierarchical Composite Properties of Cortical Bone: A Transgenic Approach [PhD thesis]. University of Michigan; 1994.
1995	Tseng K-F. Investigating the Structure-Function Relationships of Long Bone: An Approach Using Growth Hormone Mouse Models [PhD thesis]. University of Michigan; 1995.
2015	Begun DL. Age-Related Changes in Bone: Variation and Factors Influencing Bone Fragility [PhD thesis]. University of Michigan; 2015.
1981	Ruff CB. Structural Changes in the Lower Limb Bones With Aging At Pecos Pueblo [PhD thesis]. Philadelphia, PA: University of Pennsylvania; 1981.
1998	Vajda EG. Age-Related Changes in the Microstructure and Mineralization of the Female Proximal Femur [PhD thesis]. University of Utah; March 1998.
2017	Gooding AF. Variation in Cortical Bone Distribution in the Aging Adult Appendicular Skeleton [PhD thesis]. Knoxville, University of Tennessee; December 2017.
2003	Cormier JM. Microstructural and Mechanical Properties of Human Ribs [Master's thesis]. Virginia Polytechnic Institute and State University; April 22, 2003.
2017	Meng Y. Development and Validation of a Child Finite Element Model for Use in Pedestrian Accident Simulations [Master's thesis]. Virginia Polytechnic Institute and State University; April 28, 2017.